Abstract
At present, the concentration of environmental pollutants, such as pesticides and antibiotics exposed in environment, especially in aquatic environment is increasing. Research on environmental pollutants has exploded in the last few years. However, studies on the combined effects of pesticides and antibiotics on fish are rare, especially the toxic damage to gill tissue is vague. In this paper, cypermethrin (CMN) and sulfamethoxazole (SMZ) were analyzed and found that there was a strong correlation between the pathways affected by the first 30 genes regulated by CMN and SMZ, respectively. Therefore, the toxic effects of CMN (0.651 μg L−1) and/or SMZ (0.3 μg L−1) on grass carp gill were studied in this paper. Histopathology, quantitative real-time PCR, and other methods were used to detect the tissue morphology, oxidative stress level, inflammation, and apoptosis-related indicators of the fish gills after exposure of 42 days. It was found that compared with the single exposure (CMN/SMZ) group, the combined exposure (MIX) group had a more pronounced oxidative stress index imbalance. At the same time, nuclear factor-κB (NF-κB) signal pathway was activated and immuno-inflammatory reaction appeared in MIX group. The expression of tumor necrosis factor (TNF-α) in the rising range is 2.94 times that of the C group, while the expression of interleukin 8 (IL-8) is as high as 32.67 times. This study reveals the harm of CMN and SMZ to fish, and provides a reference and basis for the rational use of pesticides and antibiotics.
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References
Aderemi AO, Novais SC, Lemos MFL, Alves LM, Hunter C, Pahl O (2018) Oxidative stress responses and cellular energy allocation changes in microalgae following exposure to widely used human antibiotics. Aquat Toxicol 203:130–139. https://doi.org/10.1016/j.aquatox.2018.08.008
Aldini G, Altomare A, Baron G, Vistoli G, Carini M, Borsani L et al (2018) N-acetylcysteine as an antioxidant and disulphide breaking agent: the reasons why. Free Radic Res 52:751–762. https://doi.org/10.1080/10715762.2018.1468564
Arab-Nozari M, Mohammadi E, Shokrzadeh M, Ahangar E, Amiri FT, Shaki F (2020) Co-exposure to non-toxic levels of cadmium and fluoride induces hepatotoxicity in rats via triggering mitochondrial oxidative damage, apoptosis, and NF-kB pathways. Environ Sci Pollut R 27:24048–24058. https://doi.org/10.1007/s11356-020-08791-4
Balkwill F (2006) TNF-alpha in promotion and progression of cancer. Cancer Metast Rev 25:409–416. https://doi.org/10.1007/s10555-006-9005-3
Bedi JS, Gill JPS, Aulakh RS, Kaur P, Sharma A, Pooni PA (2013) Pesticide residues in human breast milk: risk assessment for infants from Punjab, India. Sci Total Environ 463:720–726. https://doi.org/10.1016/j.scitotenv.2013.06.066
Bedi JS, Gill JPS, Aulakh RS, Kaur P (2015) Pesticide residues in bovine milk in Punjab, India: spatial variation and risk assessment to human health. Arch Environ Con Tox 69:230–240. https://doi.org/10.1007/s00244-015-0163-6
Bellezza I, Giambanco I, Minelli A, Donato R (2018) Nrf2-keap1 signaling in oxidative and reductive stress. Bba-Mol Cell Res 1865:721–733. https://doi.org/10.1016/j.bbamcr.2018.02.010
Casalino E, Calzaretti G, Landriscina M, Sblano C, Fabiano A, Landriscina C (2007) The Nrf2 transcription factor contributes to the induction of alpha-class GST isoenzymes in liver of acute cadmium or manganese intoxicated rats: comparison with the toxic effect on NAD(P)H: quinone reductase. Toxicology 237:24–34. https://doi.org/10.1016/j.tox.2007.04.020
Chen D, Ning F, Zhang J, Tang Y, Teng X (2020a) NF-kappaB pathway took part in the development of apoptosis mediated by miR-15a and oxidative stress via mitochondrial pathway in ammonia-treated chicken splenic lymphocytes. Sci Total Environ 729:139017. https://doi.org/10.1016/j.scitotenv.2020.139017
Chen H, Liu S, Xu XR, Zhou GJ, Liu SS, Yue WZ et al (2015) Antibiotics in the coastal environment of the Hailing Bay region, South China Sea: spatial distribution, source analysis and ecological risks. Mar Pollut Bull 95:365–373. https://doi.org/10.1016/j.marpolbul.2015.04.025
Chen H, Liu S, Xu XR, Diao ZH, Sun KF, Hao QW et al (2018) Tissue distribution, bioaccumulation characteristics and health risk of antibiotics in cultured fish from a typical aquaculture area. J Hazard Mater 343:140–148. https://doi.org/10.1016/j.jhazmat.2017.09.017
Chen K, Zhou JL (2014) Occurrence and behavior of antibiotics in water and sediments from the Huangpu River, Shanghai, China. Chemosphere 95:604–612. https://doi.org/10.1016/j.chemosphere.2013.09.119
Chen QM, Maltagliati AJ (2018) Nrf2 at the heart of oxidative stress and cardiac protection. Physiol Genomics 50:77–97. https://doi.org/10.1152/physiolgenomics.00041.2017
Chen X, Han K, Zhang T, Qi GQ, Jiang ZY, Hu CY (2020b) Grass carp (Ctenopharyngodon idella) Nrf2 alleviates the oxidative stress and enhances cell viability through upregulating the expression of HO-1. Fish Physiol Biochem 46:417–428. https://doi.org/10.1007/s10695-019-00729-z
Chi QR, Chi X, Hu XY, Wang S, Zhang HF, Li S (2018) The effects of atmospheric hydrogen sulfide on peripheral blood lymphocytes of chickens: perspectives on inflammation, oxidative stress and energy metabolism. Environ Res 167:1–6. https://doi.org/10.1016/j.envres.2018.06.051
Chi QR, Hu XY, Zhao B, Zhang Q, Zhang KX, Li S (2021) Regulation of H2S-induced necroptosis and inflammation in broiler bursa of Fabricius by the miR-15b-5p/TGFBR3 axis and the involvement of oxidative stress in this process. J Hazard Mater 406. https://doi.org/10.1016/j.jhazmat.2020.124682
Copple IM, Goldring CE, Kitteringham NR, Park BK (2008) The Nrf2-Keap1 defence pathway: role in protection against drug-induced toxicity. Toxicology 246:24–33. https://doi.org/10.1016/j.tox.2007.10.029
Cupic Miladinovic D, Prevendar Crnic A, Pekovic S, Dacic S, Ivanovic S, Santibanez JF et al (2021) Recovery of brain cholinesterases and effect on parameters of oxidative stres and apoptosis in quails (Coturnix japonica) after chlorpyrifos and vitamin B1 administration. Chem Biol Interact 333:109312. https://doi.org/10.1016/j.cbi.2020.109312
David JA, Rifkin WJ, Rabbani PS, Ceradini DJ (2017) The Nrf2/Keap1/are pathway and oxidative stress as a therapeutic target in type II diabetes mellitus. J Diabetes Res. https://doi.org/10.1155/2017/4826724
Edlich F (2018) Bcl-2 proteins and apoptosis: recent insights and unknowns. Biochem Bioph Res Co 500:26–34. https://doi.org/10.1016/j.bbrc.2017.06.190
Edwards R, Millburn P, Hutson DH (1986) Comparative toxicity of cis-cypermethrin in rainbow trout, frog, mouse, and quail. Toxicol Appl Pharmacol 84:512–522. https://doi.org/10.1016/0041-008x(86)90256-5
Elzagallaai AA, Sultan EA, Bend JR, Abuzgaia AM, Loubani E, Rieder MJ (2020) Role of oxidative stress in hypersensitivity reactions to sulfonamides. J Clin Pharmacol 60:409–421. https://doi.org/10.1002/jcph.1535
Fan TJ, Han LH, Cong RS, Liang J (2005) Caspase family proteases and apoptosis. Acta Biochim Biophys Sin Shanghai 37:719–727. https://doi.org/10.1111/j.1745-7270.2005.00108.x
Fang Y, Yang L, He J (2021) Plantanone C attenuates LPS-stimulated inflammation by inhibiting NF-kappaB/iNOS/COX-2/MAPKs/Akt pathways in RAW 264.7 macrophages. Biomed Pharmacother 143:112104. https://doi.org/10.1016/j.biopha.2021.112104
Fiedler S, Wunnemann H, Hofmann I, Theobalt N, Feuchtinger A, Walch A, et al (2020) A practical guide to unbiased quantitative morphological analyses of the gills of rainbow trout (Oncorhynchus mykiss) in ecotoxicological studies. Plos One. https://doi.org/10.1371/journal.pone.0243462
Fuller N, Magnuson JT, Hartz KEH, Fulton CA, Whitledge GW, Acuna S et al (2021) Effects of dietary cypermethrin exposure on swimming performance and expression of lipid homeostatic genes in livers of juvenile Chinook salmon, Oncorhynchus tshawytscha. Ecotoxicology 30:257–267. https://doi.org/10.1007/s10646-021-02352-2
Guerin DJ, Kha CX, Tseng KA (2021) From cell death to regeneration: rebuilding after injury. Front Cell Dev Biol 9:655048. https://doi.org/10.3389/fcell.2021.655048
Guo DM, Liu WP, Yao TS, Ma MM, Wang Q, Qiu J, et al (2021) Combined endocrine disruptive toxicity of malathion and cypermethrin to gene transcription and hormones of the HPG axis of male zebrafish (Danio rerio). Chemosphere. https://doi.org/10.1016/j.chemosphere.2020.128864
Guo JM, Xing HJ, Chen MH, Wang W, Zhang HF, Xu SW (2019) H2S inhalation-induced energy metabolism disturbance is involved in LPS mediated hepatocyte apoptosis through mitochondrial pathway. Sci Total Environ 663:380–386. https://doi.org/10.1016/j.scitotenv.2019.01.360
Harada K (2018) Antibiotic residue in environmental water in Vietnam. Yakugaku Zasshi 138:271–275
Huynh TT, Silvestre F, Nguyen TP, Kestemont P (2010) Effects of pesticides and antibiotics on penaeid shrimp with special emphases on behavioral and biomarker responses. Environ Toxicol Chem 29:929–938. https://doi.org/10.1002/etc.99
Ince S, Kucukkurt I, Demirel HH, Arslan-Acaroz D, Varol N (2020) Boron, a trace mineral, alleviates gentamicin-induced nephrotoxicity in rats. Biol Trace Elem Res 195:515–524. https://doi.org/10.1007/s12011-019-01875-4
Ji CY, Magnuson JT, Zhang W, Zhao MR (2021) New insight into the enantioselective cytotoxicity of cypermethrin: imbalance between cell cycle and apoptosis. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2020.123893
Ji PY, Li ZY, Wang H, Dong JT, Li XJ, Yi HL (2019) Arsenic and sulfur dioxide co-exposure induce renal injury via activation of the NF-kappaB and caspase signaling pathway. Chemosphere 224:280–288. https://doi.org/10.1016/j.chemosphere.2019.02.111
Kaspar JW, Niture SK, Jaiswal AK (2009) Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radical Bio Med 47:1304–1309. https://doi.org/10.1016/j.freeradbiomed.2009.07.035
Kaspar JW, Jaiswal AK (2010) Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression. J Biol Chem 285:153–162. https://doi.org/10.1074/jbc.M109.040022
Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA et al (2018) Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. P Natl Acad Sci USA 115:E3463–E3470. https://doi.org/10.1073/pnas.1717295115
Kwon B, Kho Y, Kim PG, Ji K (2016) Thyroid endocrine disruption in male zebrafish following exposure to binary mixture of bisphenol AF and sulfamethoxazole. Environ Toxicol Pharmacol 48:168–174. https://doi.org/10.1016/j.etap.2016.10.018
Li SZ, Jiang LQ, Beckmann K, Hojen JF, Pessara U, Powers NE, et al (2021) A novel anti-human IL-1R7 antibody reduces IL-18-mediated inflammatory signaling. J Biol Chem. https://doi.org/10.1016/j.jbc.2021.100630
Limbu SM, Zhou L, Sun SX, Zhang ML, Du ZY (2018) Chronic exposure to low environmental concentrations and legal aquaculture doses of antibiotics cause systemic adverse effects in Nile tilapia and provoke differential human health risk. Environ Int 115:205–219. https://doi.org/10.1016/j.envint.2018.03.034
Liu JY, Wei TZ, Wu X, Zhong HB, Qiu WH, Zheng Y (2020) Early exposure to environmental levels of sulfamethoxazole triggers immune and inflammatory response of healthy zebrafish larvae. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.134724
Lu MC, Ji JA, Jiang ZY, You QD (2016) The Keap1-Nrf2-ARE pathway as a potential preventive and therapeutic target: an update. Med Res Rev 36:924–963. https://doi.org/10.1002/med.21396
Lushchak OV, Kubrak OI, Storey JM, Storey KB, Lushchak VI (2009) Low toxic herbicide roundup induces mild oxidative stress in goldfish tissues. Chemosphere 76:932–937. https://doi.org/10.1016/j.chemosphere.2009.04.045
Martin FL, Martinez EZ, Stopper H, Garcia SB, Uyemura SA, Kannen V (2018) Increased exposure to pesticides and colon cancer: early evidence in Brazil. Chemosphere 209:623–631. https://doi.org/10.1016/j.chemosphere.2018.06.118
Moreno-Sanchez R, Marin-Hernandez A, Gallardo-Perez JC, Vazquez C, Rodriguez-Enriquez S, Saavedra E (2018) Control of the NADPH supply and GSH recycling for oxidative stress management in hepatoma and liver mitochondria. Bba-Bioenergetics 1859:1138–1150. https://doi.org/10.1016/j.bbabio.2018.07.008
Omwenga M, Kanja L, Nguta J, Mbaria J, Irungu P (2016) Assessment of organochlorine pesticide residues in farmed fish in Machakos and Kiambu counties, Kenya. Toxicol Lett 258:S176–S177. https://doi.org/10.1016/j.toxlet.2016.06.1658
Qiu SN, Fu HY, Zhou RY, Yang Z, Bai GD, Shi BM (2020) Toxic effects of glyphosate on intestinal morphology, antioxidant capacity and barrier function in weaned piglets. Ecotox Environ Safe. https://doi.org/10.1016/j.ecoenv.2019.109846
Qu W, Du GL, Feng B, Shao H (2019) Effects of oxidative stress on blood pressure and electrocardiogram findings in workers with occupational exposure to lead. J Int Med Res 47:2461–2470. https://doi.org/10.1177/0300060519842446
Ragusa MA, Costa S, Cuttitta A, Gianguzza F, Nicosia A (2017) Coexposure to sulfamethoxazole and cadmium impairs development and attenuates transcriptional response in sea urchin embryo. Chemosphere 180:275–284. https://doi.org/10.1016/j.chemosphere.2017.04.030
Raszewski G, Lemieszek MK, Lukawski K, Juszczak M, Rzeski W (2015) Chlorpyrifos and cypermethrin induce apoptosis in human neuroblastoma cell line SH-SY5Y. Basic Clin Pharmacol 116:158–167. https://doi.org/10.1111/bcpt.12285
Rosety-Rodriguez M, Ordonez FJ, Rosety M, Rosety JM, Rosety I, Ribelles A et al (2002) Morpho-histochemical changes in the gills of turbot, Scophthalmus maximus L., induced by sodium dodecyl sulfate. Ecotoxicol Environ Saf 51:223–228. https://doi.org/10.1006/eesa.2001.2148
Sakamoto T, Imai H (2017) Hydrogen peroxide produced by superoxide dismutase SOD-2 activates sperm in caenorhabditis elegans. J Biol Chem 292:14804–14813. https://doi.org/10.1074/jbc.M117.788901
Salamat N, Soleimani Z, Safahieh A, Savari A, Ronagh MT (2013) Using histopathological changes as a biomarker to trace contamination loading of Musa creeks (Persian gulf). Toxicol Pathol 41:913–920. https://doi.org/10.1177/0192623312468515
Sendra M, Pereiro P, Figueras A, Novoa B (2021) An integrative toxicogenomic analysis of plastic additives. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2020.124975
Siddiqui WA, Ahad A, Ahsan H (2015) The mystery of Bcl2 family: Bcl-2 proteins and apoptosis: an update. Arch Toxicol 89:289–317. https://doi.org/10.1007/s00204-014-1448-7
Soltanian S, Fereidouni MS (2017) Immunotoxic responses of chronic exposure to cypermethrin in common carp. Fish Physiol Biochem 43:1645–1655. https://doi.org/10.1007/s10695-017-0399-3
Sparks TC, Storer N, Porter A, Slater R, Nauen R (2021) Insecticide resistance management and industry: the origins and evolution of the insecticide resistance action committee (IRAC) and the mode of action classification scheme. Pest Manag Sci 77:2609–2619. https://doi.org/10.1002/ps.6254
Tsikas D (2017) Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: analytical and biological challenges. Anal Biochem 524:13–30. https://doi.org/10.1016/j.ab.2016.10.021
Wang Y, Zhao H, Shao Y, Liu J, Li J, Xing M (2017a) Copper or/and arsenic induce oxidative stress-cascaded, nuclear factor kappa B-dependent inflammation and immune imbalance, trigging heat shock response in the kidney of chicken. Oncotarget 8:98103–98116. https://doi.org/10.18632/oncotarget.21463
Wang Y, Zhao H, Shao Y, Liu J, Li J, Xing MJO (2017b) Copper or/and arsenic induce oxidative stress-cascaded, nuclear factor kappa B-dependent inflammation and immune imbalance, trigging heat shock response in the kidney of chicken. Oncotarget 8:98103–98116
Wang SR, Salamova A, Hites RA, Venier M (2018) Spatial and seasonal distributions of current use pesticides (CUPs) in the atmospheric particulate phase in the Great Lakes region. Environ Sci Technol 52:6177–6186. https://doi.org/10.1021/acs.est.8b00123
Wang F, Zheng FF, Liu F (2020a) Effects of triclosan on antioxidant- and apoptosis-related genes expression in the gill and ovary of zebrafish. Exp Anim Tokyo 69:199–206. https://doi.org/10.1538/expanim.19-0115
Wang Y, Zhao H, Liu Y, Nie X, Xing M (2020b) Zinc exerts its renal protection effect on arsenic-exposed common carp: a signaling network comprising Nrf2, NF-kappaB and MAPK pathways. Fish Shellfish Immunol 104:383–390. https://doi.org/10.1016/j.fsi.2020.06.031
Wang Y, Zhao HJ, Guo MH, Fei DX, Zhang LN, Xing MW (2020c) Targeting the miR-122/PKM2 autophagy axis relieves arsenic stress. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2019.121217
Wang HX, Zhang R, Li Z, Wang LS, Yu Y, Wang Q et al (2021a) Cypermethrin induces sertoli cell apoptosis through mitochondrial pathway associated with calcium. Toxicol Res (Camb) 10:742–750. https://doi.org/10.1093/toxres/tfab056
Wang T, Ma M, Chen C, Yang X, Qian Y (2021b) Three widely used pesticides and their mixtures induced cytotoxicity and apoptosis through the ROS-related caspase pathway in HepG2 cells. Food Chem Toxicol 152:112162. https://doi.org/10.1016/j.fct.2021.112162
Wang X, Yuwen T, Yanqin T (2021c) Mangiferin inhibits inflammation and cell proliferation, and activates proapoptotic events via NF-kappaB inhibition in DMBA-induced mammary carcinogenesis in rats. J Environ Pathol Toxicol Oncol 40:1–9. https://doi.org/10.1615/JEnvironPatholToxicolOncol.2021036057
Wang Y, Zhao HJ, Liu YC, Li JY, Nie XP, Huang PY, et al (2021d) Environmentally relevant concentration of sulfamethoxazole-induced oxidative stress-cascaded damages in the intestine of grass carp and the therapeutic application of exogenous lycopene. Environ Pollut. https://doi.org/10.1016/j.envpol.2021.116597
Wang Y, Zhao HJ, Mu MY, Guo MH, Xing MW (2021e) Zinc offers splenic protection through suppressing PERK/IRE1-driven apoptosis pathway in common carp (Cyprinus carpio) under arsenic stress. Ecotox Environ Safe. https://doi.org/10.1016/j.ecoenv.2020.111473
Xie SW, Yin P, Tian LX, Liu YJ, Tan BP, Niu J (2020) Interactions between dietary lipid levels and chronic exposure of legal aquaculture dose of sulfamethoxazole in juvenile largemouth bass Micropterus salmoides. Aquat Toxicol. https://doi.org/10.1016/j.aquatox.2020.105670
Ying GG, He LY, Ying AJ, Zhang QQ, Liu YS, Zhao JL (2017) China must reduce its antibiotic use. Environ Sci Technol 51:1072–1073. https://doi.org/10.1021/acs.est.6b06424
Zhang YM, Hang Y, Bing S, Hua X, Bo H, Liu HG, et al. Antagonistic effect of VDR/CREB1 pathway on cadmium-induced apoptosis in porcine spleen. Ecotox Environ Safe, 2021. 209. ARTN 111819. https://doi.org/10.1016/j.ecoenv.2020.111819
Zhao H, Wang Y, Mu M, Guo M, Yu H, Xing M (2020a) Lycopene alleviates sulfamethoxazole-induced hepatotoxicity in grass carp (Ctenopharyngodon idellus) via suppression of oxidative stress, inflammation and apoptosis. Food Funct 11:8547–8559. https://doi.org/10.1039/d0fo01638a
Zhao H, Wang Y, Guo M, Liu Y, Yu H, Xing M (2021a) Environmentally relevant concentration of cypermethrin or/and sulfamethoxazole induce neurotoxicity of grass carp: involvement of blood-brain barrier, oxidative stress and apoptosis. Sci Total Environ 762:143054. https://doi.org/10.1016/j.scitotenv.2020.143054
Zhao H, Wang Y, Liu Y, Yin K, Wang D, Li B et al (2021b) ROS-induced hepatotoxicity under cypermethrin: involvement of the crosstalk between Nrf2/Keap1 and NF-kappaB/ikappaB-alpha pathways regulated by proteasome. Environ Sci Technol 55:6171–6183. https://doi.org/10.1021/acs.est.1c00515
Zhao HJ, Wang Y, Guo MH, Mu MY, Yu HX, Xing MW (2020b) Grass carps co-exposed to environmentally relevant concentrations of cypermethrin and sulfamethoxazole bear immunodeficiency and are vulnerable to subsequent aeromonas hydrophila infection. Environ Pollut. https://doi.org/10.1016/j.envpol.2020.115156
Zhao LL, Tang G, Xiong C, Han SS, Yang CP, He K, et al (2021) Chronic chlorpyrifos exposure induces oxidative stress, apoptosis and immune dysfunction in largemouth bass (Micropterus salmoides). Environ Pollut. https://doi.org/10.1016/j.envpol.2021.117010
Zhong RZ, Fang Y, Qin GX, Li HY, Zhou DW (2015) Tea catechins protect goat skeletal muscle against H(2)O(2)-induced oxidative stress by modulating expression of phase 2 antioxidant enzymes. J Agric Food Chem 63:7921–7928. https://doi.org/10.1021/acs.jafc.5b00816
Zhou LH, Zhou MQ, Tan HD, Xiao MX (2020) Cypermethrin-induced cortical neurons apoptosis via the Nrf2/are signaling pathway. Pestic Biochem Phys. https://doi.org/10.1016/j.pestbp.2020.02.013
Zhou LH, Chang JR, Zhao WH, Gao YL (2021) Proanthocyanidins regulate the Nrf2/are signaling pathway and protect neurons from cypermethrin-induced oxidative stress and apoptosis. Pestic Biochem Phys. https://doi.org/10.1016/j.pestbp.2021.104898
Zhou LJ, Wu QLL, Zhang BB, Zhao YG, Zhao BY (2016) Occurrence, spatiotemporal distribution, mass balance and ecological risks of antibiotics in subtropical shallow Lake Taihu, China. Environ Sci-Proc Imp 18:500–513. https://doi.org/10.1039/c6em00062b
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This work was supported by the Key Projects of Natural Science Foundation of Heilongjiang Province of China (Grant ZD2020C005).
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Baoying Li: writing — original draft, visualization; Yu Wang: methodology, conceptualization; Hongjing Zhao: data curation, investigation; Kai Yin: project administration; Yachen Liu: resources; Dongxu Wang: visualization; Hui Zong: supervision; Mingwei Xing: funding acquisition.
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Li, B., Wang, Y., Zhao, H. et al. Oxidative stress is involved in the activation of NF-κB signal pathway and immune inflammatory response in grass carp gill induced by cypermethrin and/or sulfamethoxazole. Environ Sci Pollut Res 29, 19594–19607 (2022). https://doi.org/10.1007/s11356-021-17197-9
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DOI: https://doi.org/10.1007/s11356-021-17197-9